Early caregiver burden in owners of pets with suspected cancer: Owner psychosocial outcomes, communication behavior, and treatment factors

Abstract Background Owners of companion animals with serious illnesses are likely to experience “caregiver burden.” This topic has not been fully evaluated in veterinary oncology. Objectives To examine owners of a dog or cat with suspected cancer for relationships between early caregiver burden and (a) psychosocial factors: depression, stress, and quality of life; (b) owner communication behavior; and (c) specific pet treatment plan factors. Animals None. Methods This cross‐sectional, observational study recruited 164 owners of a cat or dog presenting for evaluation by a veterinary oncology service at a single referral institution. Measures of caregiver burden, psychosocial function, treatment plan elements, and demographics were collected online via owner self‐report. Medical records were reviewed to identify factors including diagnosis, medications, treatment schedules, and owner communications. Results Caregiver burden correlated with higher stress (r s = 0.40, P < .001), greater symptoms of depression (r s = 0.50, P < .001), and lower quality of life (r s = 0.39, P < .001). Pet treatment plan factors related to caregiver burden included changes in care routines, perception that compliance with new routines was challenging, and difficulty adhering to medication routines. There was low correlation between caregiver burden and owner‐driven communications (r s = 0.15, P = .07). Conclusions and Clinical Importance Findings suggest caregiver burden is similar in owners of pets with cancer and owners of pets with other diseases. Caregiver burden is present in the earliest stages of disease. Major correlates of burden including life‐disruptive treatments and schedules provide key areas for potential intervention by veterinary teams.

is present in the earliest stages of disease. Major correlates of burden including lifedisruptive treatments and schedules provide key areas for potential intervention by veterinary teams.

K E Y W O R D S
burden transfer, client factors, neoplasia, quality of life

| INTRODUCTION
Recent work indicates that companion animal owners experience depressive symptoms after a diagnosis of cancer in the animal. 1 While depressive symptoms might be related to anticipated bereavement, so-called "anticipatory grief," 1,2 they might also be due in part to "caregiver burden." 3 Caregiver burden is a term traditionally used in human medicine to describe an individual's response to the challenges presented by caring for a sick human family member, and is related to poorer psychological and physiologic outcomes for the caregiver. [4][5][6][7] Caregiver burden has been recently documented in individuals caring for sick companion animals, particularly animals with chronic or terminal illnesses. 8,9 In these studies, burden was related to poor psychosocial functioning, including clinically meaningful levels of depressive symptoms and reduced quality of life. 8,9 There is a link between caregiver burden and specific elements of the companion animal's treatment plan, including several factors that the veterinary team can influence. For example, owners who report that their companion animal's disease management requires a major change to their daily routine or who feel like it is hard to adjust to these new routines report higher burden. 9 Moreover, owners who experience higher burden are more likely to demonstrate certain behaviors in the context of interacting with their veterinary care team, including more frequent communications, 9 conflict-involving interactions, or both. 10 These behaviors are in turn important contributors to veterinarian stress and burnout. 10 Whether or not a companion animal develops cancer and whether that cancer is life-threatening are things that cannot be changed. However, how an owner understands the situation, and what impact the diagnosis has on that individual's day-to-day life are things that the veterinary team can have significant influence over. Knowing how specific treatment factors affect caregiver burden and psychosocial well-being could influence how the veterinary team approaches treatment planning and allow clinicians to employ strategies to reduce burden.
The purpose of our study was to examine owners of companion animals with suspected cancer evaluated by an oncology service at a referral hospital, as these owners represent a unique demographic relative to owners previously studied, 8,9 for the relationship between burden and (a) psychosocial factors of depressive symptoms, stress, and quality of life, (b) clinic communication behavior, and (c) specific factors of treatment plan complexity including subjective experience (eg, difficulty adjusting to new routines) and objective report (eg, number and frequency of medications). We hypothesized that higher burden would be associated with poorer psychosocial functioning, greater owner-driven communication with the clinic, and changes or challenges in the treatment plan.

This research was conducted and reported in accordance with
Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) criteria. 11 The study protocol was reviewed and approved by the institutional review boards (IRBs) of Purdue University and Kent State University. All participants provided informed consent for study participation.

| Sample
Participants were owners of newly registered dogs and cats evaluated by the oncology service at a large academic specialty hospital. Inclusion criteria to enroll in the study were that the participant must be ≥18 years of age, able to comprehend and respond to questions in English, and currently living with and providing care for a dog or cat presenting to the center for diagnosis and possible treatment. Exclusion criteria included failure to complete the protocol (ie, beginning the protocol but discontinuing before the end). Participants were not excluded if they completed the protocol but declined to answer specific questions as this was an option required by the IRB.

| Record review
Data extraction from veterinary records was conducted by the research team (Purdue University and Kent State University). Data from the time of the initial visit (when questionnaires were completed) were retrieved for: (a) diagnosis, (b) number of daily medications prescribed (number), (c) times per day the pet receives medication (number), (d) whether the pet was prescribed a new medication for presenting diagnosis before referral (yes/no), (e) whether the pet was prescribed a new medication that required a schedule change, or had a schedule change to an existing medication before referral, for presenting diagnosis (yes/no), (f) estimated treatment cost (number), and (g) miles from caregiver's home address to treatment center (number).
In addition, number of incoming telephone contacts (no inbound email, text, or other communication method to the clinic was available to clients at the time) from the owner to the service in the 30 days after study enrollment were counted. The 30-day period after the initial meeting was selected for the purposes of retention, as several of the presenting conditions were terminal.

| Study measures and instruments
A brief description of measures is presented below; the purpose and psychometric properties of these instruments have been described in greater detail. 8,9 All scoring of questionnaires was conducted in aggregate and in accordance with measure instructions.

| Caregiver burden
The Zarit Burden Interview (ZBI) 3 adapted for use with companion animals 8 includes 18 items rated on a scale of 0 (never) to 4 (nearly always).
Questions reflect subjective (eg, feelings of guilt, anger, frustration) and objective (eg, physical health, social life, financial impact) burdens of caregiving. Example subjective questions include "Do you feel angry when you are around your pet?" and "Do you feel embarrassed over your pet's behavior?" 8 Example objective questions include "Do you feel your health has suffered because of your involvement with your pet?" and "Do you feel that you don't have enough money to care for your relative in addition to the rest of your expenses?" 8 Higher scores indicate greater level of burden. A cutoff of 18 on the ZBI adapted for use with companion animals indicates clinically meaningful caregiver burden. 8 Cronbach's α for the current sample was α = .89.

| Perceived stress
The Perceived Stress Scale 12 is a 10-item scale addressing degree of current stress on scale of 0 (never) to 4 (very often) with reversal of item scores as indicated. Items ask about frequency of feelings of being nervous, stressed, and difficulty controlling irritation. There is not a standard cutoff to indicate increased perceived stress. Scores typically range from 12 to 14 (range of possible scores, 0-40), with higher scores indicating higher levels of stress. 9 Cronbach's α for the current sample was α = .91.

| Depressive symptoms
The Center for Epidemiology Studies Depression scale 13  were used, as previously described. 9 Two items that are not included in total scoring were omitted, and a third item was removed due to sensitive content not considered integral to the research question. No cutoff exists for this measure; however, higher score indicates better quality of life, and the measure has evidence of acceptable psychometric properties. 9 Cronbach's α for the current sample was α = .95.

| Treatment factors
Selected items from the pet owner adherence scale (POAS) 16 were utilized. The POAS is a measure of owner perceptions of a companion animal's disease and treatment. Although designed to examine adherence, this scale addresses several issues relevant to caregiving for a companion animal, including treatment needs and owners' subjective perceptions of the treatment. Seven (7) items related to how well the owner feels the companion animal's disease, medications, and treatment routines have been explained, and how difficult it is to comply with treatment regimens were utilized. Responses are scored on a scale of 1 (strongly disagree) to 5 (strongly agree). No cutoff exists for this measure; however, higher scores indicate greater perceived difficulty related to the treatment plan. Cronbach's α for the selected items used in the current sample was α = .71.

| Recruitment and data collection procedures
Data were collected between July 2018 and March 2019 for this cross-sectional, observational study. All participants were owners registering a new companion animal (cat or dog) for evaluation and potential treatment with the above-described oncology service.
Owners were asked by clinical staff about their interest in research participation during the clinical evaluation. Interested individuals then discussed enrollment in the study with a research assistant. Owners who agreed to participate were asked to provide informed consent to complete study questionnaires and allow research personnel to extract information from the pet's records. They were provided an electronic device equipped with a Qualtrics-based instrument including the above-described measures, and were asked to complete measures during "down time" at their companion animal's appointment.
Any owners willing to participate but unable to complete measures during this period were sent an email link to the protocol to complete it remotely online. Participation was solely on a volunteer basis, and was not reimbursed.

| Power analysis
Prior work examining caregiver burden in owners of companion animals 8-10 demonstrated that the adapted ZBI correlates with measures of depression, stress, quality of life, difficulty of the treatment plan, and nonbillable owner contacts between r = 0.31 to 0.59. Using a significance level of α = .05 and power π = 0.8 for a medium effect (r = 0.30), a conservative sample size of 85 participants was needed.
Over-sampling was planned due to the expectation that the current sample would consist largely of owners presenting their companion animals early in the disease process, which could be associated with lower overall levels of caregiver burden. 17 Table 1 for sample demographic make-up. For analyses involving owner-driven communications, a further exclusion for no diagnosis of cancer (n = 11) was applied for a total of 153 in this subsample, as these individuals would have no reason to continue with the oncology service.

| Caregiver burden and psychosocial function
Descriptive statistics for each questionnaire are shown in Table 2.
Spearman rank-order correlation analyses in the full sample revealed significant relationships between adapted ZBI scores and scores for each of the psychosocial function questionnaires (P < .001 for all; Table 2). Greater caregiver burden was associated with greater symptoms of depression (r s = 0.50), higher levels of perceived stress (r s = 0.40), and lower quality of life (r s = 0.39).

| Caregiver burden and frequency of ownerdriven communications
In the subset of owners whose companion animal was diagnosed with cancer (n = 153), Spearman correlation analysis between the number of owner-driven communications in the 30 days after measure completion and adapted ZBI scores revealed a small-to-moderate association (r s = 0.15, P = .07). 19 3.4 | Caregiver burden and chart review: Treatment, cost, and treatment center distance Adapted ZBI scores and treatment variables extracted from the medical chart are presented in Table 3; correlations of the greatest magnitude were presence of medication required at the time of consult (r s = 0.14, P = .08) and number of prior medications required (r s = 0.13, P = .09). 19 See Table 3.  Table 3.

| DISCUSSION
While previous work has included owners of companion animals with cancer in a general hospital setting, 9  showed that caregiver burden correlates positively with measures of depressive symptoms and stress, and negatively with measures of quality of life. 8,9 Similarly, the small to moderate relationship 19 observed between caregiver burden and greater owner-driven communications to the clinic parallels findings from past work, 9 demonstrating a connection between the owner's caregiver burden and their communication behavior with the veterinary clinic. The magnitude of correlations in the current work suggests these relationships are meaningful, 19 but the relationship strengths detected here are generally smaller than was found in past work using a general veterinary hospital sample. 8,9 The smaller effects in our study could reflect the different disease presentations in a general hospital vs oncological setting, but might also be due to timing. Data for our study were collected at an initial appointment evaluating for possible cancer, and more than half of our sample reported duration of disease lower than 1 month. In comparison, prior work reporting similar relationships between burden and psychosocial function 8 was conducted in a sample in which the majority of owners reported duration of disease lasting a year or longer. Similarly, past work examining the relationship between caregiver burden and owner-driven communications 9 did so over the course of a full year, whereas our study only examined 30 days. Work in human samples shows that duration of disease predicts caregiver burden, 20,21 and duration of caregiving is correlated with burden in companion animal caregiving samples. 17 Average burden in the current sample was lower than has been observed in prior samples, 8,9,17 suggesting possible restricted range of burden within this sample, which would in turn impact the strength of these relationships. Importantly, directionality of these findings cannot be assumed, that is, we do not know that caregiver burden is driving owners to feel more depressed or stressed, or to make more frequent phone calls-it is possible that those with higher levels of psychosocial dysfunction and those who would have been more likely to make frequent calls are simply experiencing caregiving as more burdensome. Work from human caregiving suggests the former relationship, that is, that caregiver burden is the instigating factor, 22 but longitudinal research is needed to definitively determine directionality.
The likely impact of caregiver burden on both the owner (ie, psychosocial distress) and veterinary provider (ie, additional owner communications) underscores the importance of considering how the owner's caregiver burden might be reduced. To this end, we examined variables associated with the treatment plan. Results indicated burden was most significantly correlated with perceptions of challenge in managing new medication routines and rules, and impact of medication routines on the owner's daily schedule. In addition, the sense that medications had been explained and were effective also negatively associated with burden. Additionally, a correlation was observed between burden and whether medications were required before the diagnosis and the number of medications given for the current illness; while relatively small in magnitude, these relationships might ultimately bear important consequences. 19 These findings extend prior work, 9 in which a small sample from a general hospital clientele showed significant correlations in the relationship between caregiver burden and change in routine as a result of a companion animal's illness and perception that the routine was difficult. Our study has a larger sample relative to the previous study, which contributed greater power to detect significant relationships. Our study also extends prior work by adding the objective element of record review and more spe- The link between burden and frequent client initiated contacts suggests that implementation of a team approach including veterinary social workers and client liaisons might be beneficial for clients and in reducing the strain placed on veterinarians and technicians. 24 Moreover, acknowledging and validating the existence of burden and associated emotions provides an opportunity for the veterinary team to offer validation and understanding, and enhance collaborative caregiving with owners. 26 Limitations of the current work are acknowledged. A primary limitation is in the cross-sectional examination of owners in the earliest stages of their companion animal's illness. As noted above, because duration of care is positively related to burden, the current sample might not have had sufficient time to develop significant burden.
Issues such as having a new treatment plan, covering costs for expensive diagnostics, expensive treatment, or both, or driving a far distance to the oncology center might not have been significantly related to burden at this time point simply because they had not yet emerged as known stressors for these owners. Burden is likely to develop with time, 20,21 perhaps after the owner has received bills or repeatedly undertakes a long drive to the treatment center. Longitudinal work is needed to examine the primary contributors to development of burden in a veterinary oncology setting over time. Another limitation might be found in that participants were not consecutively enrolled clients of the oncology service, but rather, recruited on a voluntary basis during their initial visit to the oncology center. Not all individuals elected to participate in the study. The sample might include individuals who were particularly motivated to describe their experiences, which could reduce generalizability. Furthermore, because data were collected at a single referral hospital, they might not be fully representative of the population of owners of pets with cancer, as our population was comprised of mostly female (although a greater percent of male participants was included relative to past work 8 ), mostly white, mostly well-educated, and entirely English-competent individuals. Our participants were also biased strongly toward dog-ownership over cat-ownership, reflecting the population served by the referral institution, but not necessarily reflecting the population of companion animals with cancer or suspected cancer.
In summary, the current work demonstrates the existence of caregiver burden as early as the initial referral visit for caregivers of pets with cancer or suspected cancer. It also confirms relationships between burden and owner psychosocial variables, including stress, depression, and reduced quality of life, as well as potential impact on veterinary medical professionals via greater need for communication.
Major correlates of burden including life-disruptive treatments and schedules provide key areas for potential intervention by veterinary medical teams.

CONFLICT OF INTEREST DECLARATION
Authors declare no conflict of interest.

OFF-LABEL ANTIMICROBIAL DECLARATION
Authors declare no off-label use of antimicrobials.